Skip to main content
SpringerLink
Log in

New Cells of the Adult Brain and the Regulation of Social Behavior

  • Published:
Biology Bulletin Reviews Aims and scope Submit manuscript

Abstract

Studies of neural stem cells (NSCs) made substantial adjustments to the basic knowledge of brain development and function. Neurons transformed from NSCs are necessary participants in many physiological processes of the adult brain. The level of neurogenesis, its dynamics, and the number of emerging cells increase with memory stimulation, cognitive processes, social adaptation, reproductive function, and protection from stress. The article considers examples of how experience in communication with an environment of enriched informational background stimulates the formation of new neurons. The analysis makes it possible to consider neurogenesis as a new mechanism to maintain the adaptive plasticity of the adult brain.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Adlaf, E.W., Vaden, R.J., Niver, A.J., et al., Adult-born neurons modify excitatory synaptic transmission to existing neurons, eLife, 2017, vol. 6, p. e19886. doi 10.7554/eLife.19886

    Article  PubMed  PubMed Central  Google Scholar 

  • Aleksandrova, M.A. and Marei, M.V., Stem cells in the brain of mammals and human: fundamental and applied aspects, Zh. Vyssh. Nervn. Deyat. im. I.P. Pavlova, 2015, vol. 65, no. 3, pp. 1–35.

    Google Scholar 

  • Appleby, P.A., Kempermann, G., and Wiskott, L., The role of additive neurogenesis and synaptic plasticity in a hippocampal memory model with grid cell like input, PLoS Comput. Biol., 2011, vol. 7, no. 1, p. e1001063. doi 10.1371/journal.pcbi.1001063

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Barkan, S., Roll, U., Yom-Tov, Y., et al., Possible linkage between neuronal recruitment and flight distance in migratory birds, Sci. Rep., 2016, vol. 6, p. 21983. doi 10.1038/srep21983

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Barkan, S., Yom-Tov, Y., and Barnea, A., Exploring the relationship between brain plasticity, migratory lifestyle, and social structure in birds, Front. Neurosci., 2017, vol. 11, p. 139. doi 10.3389/fnins.2017.00139

    PubMed  Google Scholar 

  • Cattaneo, E. and Bonfanti, L., Therapeutic potential of neural stem cells: greater in people’s perception than in their brains?, Front. Neurosci., 2014, vol. 8, p. 79. doi 10.3389/fnins.2014.00079

    Article  PubMed  PubMed Central  Google Scholar 

  • Chancellor, L.V., Roth, T.C., LaDage, L.D., and Pravosudov, V.V., The effect of environmental harshness on neurogenesis: a large-scale comparison, Dev. Neurobiol., 2011, vol. 71, no. 3, pp. 246–252.

    Article  PubMed  PubMed Central  Google Scholar 

  • Chen, C.C., Huang, C.C., and Hsu, K.S., Chronic social stress affects synaptic maturation of newly generated neurons in the adult mouse dentate gyrus, Int. J. Neuropsychopharm., 2015, vol. 19, no. 3, art. ID pyv097. doi 10.1093/ijnp/pyv097

    Google Scholar 

  • Clelland, C.D., Choi, M., Romberg, C., et al., A functional role for adult hippocampal neurogenesis in spatial pattern separation, Science, 2009, vol. 325, pp. 210–213.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Coras, R., Siebzehnrubl, F.A., Pauli, E., et al., Low proliferation capacities of adult hippocampal stem cells correlate with memory dysfunction in humans, Brain, 2010, vol. 133, no. 11, pp. 3359–3372.

    Article  PubMed  Google Scholar 

  • Deng, W., Aimone, J.B., and Gage, F.H., New neurons and new memories: how does adult hippocampal neurogenesis affect learning and memory?, Nat. Rev. Neurosci., 2010, vol. 11, no. 5, pp. 339–350.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Deshpande, A., Bergami, M., Ghanem, A., et al., Retrograde monosynaptic tracing reveals the temporal evolution of inputs onto new neurons in the adult dentate gyrus and olfactory bulb, Proc. Natl. Acad. Sci. U.S.A., 2013, vol. 110, pp. E1152–E1161.

    Article  PubMed  PubMed Central  Google Scholar 

  • Enikolopov, G., Overstreet-Wadiche, L. and Ge, S., Viral and transgenic reporters and genetic analysis of adult neurogenesis, Cold Spring Harbor Perspect. Biol., 2015, vol. 7, no. 8, p. a018804. doi 10.1101/cshperspect.a018804

    Article  CAS  Google Scholar 

  • Feierstein, C.E., Linking adult olfactory neurogenesis to social behavior, Front. Neurosci., 2012, vol. 6, p. 173. doi 10.3389/fnins.2012.00173

    Article  PubMed  PubMed Central  Google Scholar 

  • Feierstein, C.E., Lazarini, F., Wagner, S., et al., Disruption of adult neurogenesis in the olfactory bulb affects social interaction but not maternal behavior, Front. Behav. Neurosci., 2010, vol. 4, p. 176. doi 10.3389/fnbeh.2010.00176

    Article  PubMed  PubMed Central  Google Scholar 

  • Fiore, M., Amendola, T., Triaca, V., et al., Agonistic encounters in aged male mouse potentiate the expression of endogenous brain NGF and BDNF: possible implication for brain progenitor cells’ activation, Eur. J. Neurosci., 2003, vol. 17, no. 7, pp. 1455–1464.

    Article  PubMed  Google Scholar 

  • Freund, J., Brandmaier, A.M., Lewejohann, L., et al., Emergence of individuality in genetically identical mice, Science, 2013, vol. 340, pp. 756–759.

    Article  PubMed  CAS  Google Scholar 

  • Furuta, M. and Bridges, R.S., Gestation-induced cell proliferation in the rat brain, Dev. Brain Res., 2005, vol. 156, pp. 61–66.

    Article  CAS  Google Scholar 

  • Garthe, A., Roeder, I., and Kempermann, G., Mice in an enriched environment learn more flexibly because of adult hippocampal neurogenesis, Hippocampus, 2016, vol. 26, no. 2, pp. 261–271. doi 10.1002/hipo.22520

    Article  PubMed  Google Scholar 

  • Ge, S., Yang, C.H., Hsu, K.S., et al., A critical period for enhanced synaptic plasticity in newly generated neurons of the adult brain, Neuron, 2007, vol. 54, no. 4, pp. 559–566.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Gomazkov, O.A., Neurogenesis as an adaptive function of the adult brain, Biol. Bull. Rev., 2014, vol. 4, no. 2, pp. 86–100.

    Article  Google Scholar 

  • Gould, E. and Tanapat, P., Stress and hippocampal neurogenesis, Biol. Psychiatry, 1999, vol. 46, no. 11, pp. 1472–1479.

    Article  PubMed  CAS  Google Scholar 

  • Gu, Y., Janoschka, S., and Ge, S., Neurogenesis and hippocampal plasticity in adult brain, Curr. Top. Behav. Neurosci., 2013, vol. 15, pp. 31–48.

    Article  PubMed  CAS  Google Scholar 

  • Hoffman, E., Pickavance, L., Thippeswamy, T., et al., The male sex pheromone darcin stimulates hippocampal neurogenesis and cell proliferation in the subventricular zone in female mice, Front. Behav. Neurosci., 2015, vol. 9, p. 106. doi 10.3389/fnbeh.2015.00106

    PubMed  PubMed Central  Google Scholar 

  • Hsiao, Y.H., Hung, H.C., Chen, S.H., and Gean, P.W., Social interaction rescues memory deficit in an animal model of Alzheimer’s disease by increasing BDNFdependent hippocampal neurogenesis, J. Neurosci., 2014, vol. 34, no. 49, pp. 16207–16219.

    Article  PubMed  CAS  Google Scholar 

  • Ikrar, T., Guo, N., He, K., et al., Adult neurogenesis modifies excitability of the dentate gyrus, Front. Neural. Circuits, 2013, vol. 7, p. 204. doi 10.3389/fncir.2013.00204

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Jessberger, S., Clark, R.E., Broadbent, N.J., et al., Dentate gyrus-specific knockdown of adult neurogenesis impairs spatial and object recognition memory in adult rats, Learn. Mem., 2009, vol. 16, pp. 147–154.

    Article  PubMed  PubMed Central  Google Scholar 

  • Johnston, S.T., Shtrahman, M., Parylak, S., et al., Paradox of pattern separation and adult neurogenesis: a dual role for new neurons balancing memory resolution and robustness, Neurobiol. Learn. Mem., 2016, vol. 129, pp. 60–68. doi 10.1016/j.nlm.2015.10.013

    Article  PubMed  Google Scholar 

  • Kempermann, G., Kuhn, H.G., and Gage, F.H., More hippocampal neurons in adult mice living in an enriched environment, Nature, 1997, vol. 386, no. 6624, pp. 493–495.

    Article  PubMed  CAS  Google Scholar 

  • Kempermann, G., Kuhn, H.G., and Gage, F.H., Experience-induced neurogenesis in the senescent dentate gyrus, J. Neurosci., 1998, vol. 18, pp. 3206–3212.

    Article  PubMed  CAS  Google Scholar 

  • Kitamura, T. and Inokuchi, K., Role of adult neurogenesis in hippocampal-cortical memory consolidation, Mol. Brain, 2014, vol. 7, p. 13. doi 10.1186/1756-6606-7-13

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kobayashi, M., Nakatani, T., Koda, T., et al., Absence of BRINP1 in mice causes increase of hippocampal neurogenesis and behavioral alterations relevant to human psychiatric disorders, Mol. Brain, 2014, vol. 7, p. 12. doi 10.1186/1756-6606-7-12

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kuvacheva, N.V., Morgun, A.V., Komleva, Yu.K., Khilazheva, E.D., Gorina, Ya.V., Lopatina, O.L., Arutyunyan, S.A., and Salmina, A.B., In vitro modeling of brain progenitor cell development under the effect of environmental factors, Bull. Exp. Biol. Med., 2015, vol. 159, no. 4, pp. 546–549.

    Article  PubMed  CAS  Google Scholar 

  • LaDage, L.D., Roth, T.C., and Pravosudov, V.V., Hippocampal neurogenesis is associated with migratory behaviour in adult but not juvenile sparrows, Proc. R. Soc. London, Ser. B, 2011, vol. 278, pp. 138–143.

    Article  Google Scholar 

  • LaDage, L.D., Maged, R.M., Forney, M.V., et al., Interaction between territoriality, spatial environment, and hippocampal neurogenesis in male side-blotched lizards, Behav. Neurosci., 2013, vol. 127, no. 4, pp. 555–565.

    PubMed  Google Scholar 

  • Lagace, D.C., Donovan, M.H., DeCarolis, N.A., et al., Adult hippocampal neurogenesis is functionally important for stress-induced social avoidance, Proc. Natl. Acad. Sci. U.S.A., 2010, vol. 107, no. 9, pp. 4436–4441.

    Article  PubMed  PubMed Central  Google Scholar 

  • Larsen, C.M., Kokay, I.C., and Grattan, D.R., Male pheromones initiate prolactin-induced neurogenesis and advance maternal behavior in female mice, Horm. Behav., 2008, vol. 53, pp. 509–517.

    Article  PubMed  CAS  Google Scholar 

  • Lieberwirth, C. and Wang, Z., The social environment and neurogenesis in the adult mammalian brain, Front. Hum. Neurosci., 2012, vol. 6, p. 118. doi 10.3389/fnhum.2012.00118

    Article  PubMed  PubMed Central  Google Scholar 

  • Liu, A., Jain, N., Vyas, A., and Lim, L.W., Ventromedial prefrontal cortex stimulation enhances memory and hippocampal neurogenesis in the middle-aged rats, eLife, 2015, vol. 13, p. 4. doi 10.7554/eLife.04803

    Google Scholar 

  • Lu, L., Bao, G., Chen, H., et al., Modification of hippocampal neurogenesis and neuroplasticity by social environments, Exp. Neurol., 2003, vol. 183, no. 2, pp. 600–609.

    Article  PubMed  Google Scholar 

  • Mak, G.K., Enwere, E.K., Gregg, C., et al., Male pheromone- stimulated neurogenesis in the adult female brain: possible role in mating behavior, Nat. Neurosci., 2007, vol. 10, no. 8, pp. 1003–1011.

    Article  PubMed  CAS  Google Scholar 

  • Mandairon, N., Jourdan, F., and Didier, A., Deprivation of sensory inputs to the olfactory bulb up-regulates cell death and proliferation in the subventricular zone of adult mice, Neuroscience, 2003, vol. 119, no. 2, pp. 507–516.

    Article  PubMed  CAS  Google Scholar 

  • Oboti, L., Schellino, R., Giachino, C., et al., Newborn interneurons in the accessory olfactory bulb promote mate recognition in female mice, Front. Neurosci., 2011, vol. 5, p. 113. doi 10.3389/fnins.2011.00113

    Article  PubMed  PubMed Central  Google Scholar 

  • Oomen, C.A., Mayer, J.L., de Kloet, E.R., et al., Brief treatment with the glucocorticoid receptor antagonist mifepristone normalizes the reduction in neurogenesis after chronic stress, Eur. J. Neurosci., 2007, vol. 26, no. 12, pp. 3395–3401.

    Article  PubMed  Google Scholar 

  • Opendak, M., Offit, L., Monari, P., et al., Lasting adaptations in social behavior produced by social disruption and inhibition of adult neurogenesis, J. Neurosci., 2016, vol. 36, no. 26, pp. 7027–7038. doi 10.1523/JNEUROSCI.4435-15.2016

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Pan, Y.W., Storm, D.R., and Xia, Z., Role of adult neurogenesis in hippocampus-dependent memory, contextual fear extinction and remote contextual memory: new insights from ERK5 MAP kinase, Neurobiol. Learn. Mem., 2013, vol. 105, pp. 81–92.

    PubMed  CAS  Google Scholar 

  • Peretto, P., Schellino, R., De Marchis, S., and Fasolo, A., The interplay between reproductive social stimuli and adult olfactory bulb neurogenesis, Neural Plast., 2014, art. ID 497657. doi 10.1155/2014/497657

    Google Scholar 

  • Pérez-Martín, M., Rivera, P., Blanco, E., et al., Environmental enrichment, age, and PPAR interact to regulate proliferation in neurogenic niches, Front. Neurosci., 2016, vol. 10, p. 89. doi 10.3389/fnins.2016.00089

    PubMed  Google Scholar 

  • Portillo, W., Unda, N., Camacho, F.J., et al., Sexual activity increases the number of newborn cells in the accessory olfactory bulb of male rats, Front. Neuroanat., 2012, vol. 6, p. 25. doi 10.3389/fnana.2012.00025

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Ramón y Cajal, S., Identification and Characterization of Neural Progenitor Cells in the Adult Mammalian Brain, Berlin: Springer-Verlag, 1928.

    Google Scholar 

  • Restivo, L., Niibori, Y., Mercaldo, V., et al., Development of adult-generated cell connectivity with excitatory and inhibitory cell populations in the hippocampus, J. Neurosci., 2015, vol. 35, no. 29, pp. 10600–10612.

    Article  PubMed  CAS  Google Scholar 

  • Sahay, A., Scobie, K.N., Hill, A.S., et al., Increasing adult hippocampal neurogenesis is sufficient to improve pattern separation, Nature, 2011, vol. 472, no. 7344, pp. 466–470.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Sakamoto, M., Kageyama, R., and Imayoshi, I., The functional significance of newly born neurons integrated into olfactory bulb circuits, Front. Neurosci., 2014, vol. 8, p. 121. doi 10.3389/fnins.2014.00121

    PubMed  PubMed Central  Google Scholar 

  • Schellino, R., Trova, S., Cimino, I., et al., Opposite-sex attraction in male mice requires testosterone-dependent regulation of adult olfactory bulb neurogenesis, Sci. Rep., 2016, vol. 6, p. 36063. doi 10.1038/srep36063

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Shingo, T., Gregg, C., Enwere, E., et al., Pregnancy-stimulated neurogenesis in the adult female forebrain mediated by prolactin, Science, 2003, vol. 299, no. 5603, pp. 117–120.

    Article  PubMed  CAS  Google Scholar 

  • Smagin, D.A., Park, J.H., Michurina, T.V., et al., Altered hippocampal neurogenesis and amygdalar neuronal activity in adult mice with repeated experience of aggression, Front. Neurosci., 2015, vol. 9, p. 443. doi 10.3389/fnins.2015.00443

    Article  PubMed  PubMed Central  Google Scholar 

  • Snyder, J.S. and Cameron, H.A., Could adult hippocampal neurogenesis be relevant for human behavior?, Behav. Brain Res., 2012, vol. 227, no. 2, pp. 384–390. doi 10.1016/j.bbr.2011.06.024

    Article  PubMed  Google Scholar 

  • Snyder, J.S., Soumier, A., Brewer, M., et al., Adult hippocampal neurogenesis buffers stress responses and depressive behavior, Nature, 2011, vol. 476, no. 7361, pp. 458–461.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Soloviova, O.A., Proshin, A.T., Storozheva, Z.I., and Sherstnev, V.V., Neurogenesis enhancer RO 25–6981 facilitates repeated spatial learning in adult rats, Bull. Exp. Biol. Med., 2012, vol. 154, no. 5, pp. 764–766.

    Article  CAS  Google Scholar 

  • Spalding, K.L., Bergmann, O., Alkass, K., et al., Dynamics of hippocampal neurogenesis in adult humans, Cell, 2013, vol. 153, no. 6, pp. 1219–1227.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Toni, N., Teng, E.M., Bushong, E.A., et al., Synapse formation on neurons born in the adult hippocampus, Nat. Neurosci., 2007, vol. 10, pp. 727–734.

    Article  PubMed  CAS  Google Scholar 

  • Toni, N., Laplagne, D.A., Zhao, C., et al., Neurons born in the adult dentate gyrus form functional synapses with target cells, Nat. Neurosci., 2008, vol. 11, pp. 901–907.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Wang, W., Lu, S., Li, T., et al., Inducible activation of ERK5 MAP kinase enhances adult neurogenesis in the olfactory bulb and improves olfactory function, J. Neurosci., 2015, vol. 35, no. 20, pp. 7833–7849.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Wu, M.V. and Hen, R., Functional dissociation of adultborn neurons along the dorsoventral axis of the dentate gyrus, Hippocampus, 2014, vol. 24, no. 7, pp. 751–761.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Wu, M.V., Shamy, J.L., Bedi, G., et al., Impact of social status and antidepressant treatment on neurogenesis in the baboon hippocampus, Neuropsychopharmacology, 2014, vol. 39, no. 8, pp. 1861–1871.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Yamaguchi, M. and Mori, K., Critical period for sensory experience-dependent survival of newly generated granule cells in the adult mouse olfactory bulb, Proc. Natl. Acad. Sci. U.S.A., 2005, vol. 102, no. 27, pp. 9697–9702.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Yarygin, K.N. and Yarygin, V.N., Neurogenesis in the central nervous system and the prospects of regenerative neurology, Zh. Nevropatol. Psikhiatr. im. S.S. Korsakova, 2012, vol. 112, no. 1, pp. 4–13.

    Google Scholar 

  • Yassa, M.A. and Stark, C.E., Pattern separation in the hippocampus, Trends Neurosci., 2011, vol. 4, no. 10, pp. 515–525.

    Article  CAS  Google Scholar 

  • Zhang, X.Q., Mu, J.W., Wang, H.B., et al., Increased protein expression levels of pCREB, BDNF and SDF-1/CXCR4 in the hippocampus may be associated with enhanced neurogenesis induced by environmental enrichment, Mol. Med. Rep., 2016, vol. 14, no. 3, pp. 2231–2237.

    PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Orekhovich Institute of Biomedical Chemistry, Moscow, Russia

    O. A. Gomazkov

Authors
  1. O. A. Gomazkov
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to O. A. Gomazkov.

Additional information

Original Russian Text © O.A. Gomazkov, 2018, published in Uspekhi Sovremennoi Biologii, 2018, Vol. 138, No. 1, pp. 57–67.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Gomazkov, O.A. New Cells of the Adult Brain and the Regulation of Social Behavior. Biol Bull Rev 8, 300–308 (2018). https://doi.org/10.1134/S2079086418040035

Download citation

  • Received:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S2079086418040035

Keywords

Search

Navigation